Nutrition Research Reviews (1994), 7, 205-231 205 GLUCOSINOLATES AND GLUCOSINOLATE DERIVATIVES: IMPLICATIONS FOR PROTECTION AGAINST CHEMICAL CARCINOGENESIS LIONELLE NUGON-BAUDON* AND SYLVIE RABOT Unit6 d’Ecologie et de Physiologie du Systbme Digestif, Centre de Recherches de Jouy, Institut National de la Recherche Agronomique, 78352 Jouy-en-Josas Cedex, France CONTENTS G L U COS I N 0 LAT ES : OCCURRENCE AND METABOLIC FATE . 205 GLUCOSINOLATES IN THE PLANT . 205 GENESIS OF GLUCOSINOLATE DERIVATIVES . 207 Enzymic hydrolysis and autolysis in cruciferous vegetables . 207 Bacterial metabolism of glucosinolates . 212 FROM THE PLANT TO THE DIET: INFLUENCE OF FOOD PROCESSING AND DIETARY HABITS. 213 TOXICITY OF GLUCOSINOLATES AND GLUCOSINOLATE DERIVATIVES . 215 GLUCOSINOLATES AND GLUCOSINOLATE DERIVATIVES: NEW CANDIDATES FOR PROTECTION AGAINST CHEMICAL CARCINOGENESIS . 217 EPIDEMIOLOGICAL DATA: CRUCIFEROUS VEGETABLES AND CANCER INCIDENCE IN HUMAN POPULATIONS . 217 EX PER I MENTAL DATA : CRUCIFEROUS VEGETABLES, G L U COSINOL ATES AND CHEMICAL CARCINOGENS IN ANIMAL MODELS . 217 EXPERIMENTAL DATA : CRUCIFEROUS VEGETABLES, G LU COSINOLATES AND XENOBIOTIC METABOLIZING ENZYMES . 219 The xenobiotic metabolizing enzymes . 219 The efsects of cruciferous vegetables on the XME system . 220 The efeects of glucosinolates and glucosinolate derivatives on the XME system . 222 CONCLUSIONS AND PENDING TOPICS . 224 REFERENCES . 225 GLUCOSINOLATES: OCCURRENCE AND METABOLIC FATE GLUCOSINOLATES IN THE PLANT Glucosinolates (GSL) are sulphur-containing molecules produced from amino acids by the secondary metabolism of plants. Their occurrence is limited to some families of dicotyledonous angiosperms. Considering edible plants only, they occur predominantly in Cruciferae and Capparideae and, sporadically, in Caricaceae and Tropaeolaaceae (Table 1). * Corresponding author. Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.22, on 24 Sep 2021 at 21:32:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1079/NRR19940012 206 L. NUGON-BAUDON AND SYLVIE RABOT Table 1. Glucosinolate-containing edible plants - Cruciferae Brassica oleracea L. gongylodes group Kohlrabi capitata group Red/white cabbage sabauda group Savoy cabbage gemmifera group Brussels sprouts italica group Broccoli botrytis group var. caulifora DC. Cauliflower var. cymosa Lam. Calabrese (green sprouting broccoli) acephala group var. millecapitata (Lev) Thell. Thousand head kale var. medullosa Thell. Marrowstem kale var. selensia Curly kale var. sabellica Collard Brassica alboglabra Bailey Chinese kale Brassica pekinensis (Lour.) Rupr. Chinese cabbage (Pe-tsai) Brassica chinensis L. Chinese white cabbage (Pak-choi) Brassica campestris L. ssp. rapifera (Metzg.) Sinsk. Turnip ssp. oleijera (Metzg.) Sinsk. Turnip rape Brassica napus L. var. napobrassica (L.) Peterm Swede (Rutabaga) or ssp. rapifera (Metzg.) Sinsk. var. napus Winter, summer rape Brassica nigra (L.L) Koch Black mustard Brassica juncea (L.) Czern et Coss Brown mustard Brassica carinata A. Br. Abyssinian mustard (Ethiopian cabbage) Sinapis alba L. White mustard Crambe maritima L. Sea kale Raphanus sativus L. Radish Armoracia lapathifolia Gilib Horseradish Wasabi japonica Matsum. Wasabi (Japanese horseradish) Eruca sativa (Miller) Thell. Salad rocket Lepidium sativum L. Garden cress Nasturtium officinalis R. Br. Water cress Capparaceae Capparis spinosa Caper Caricaceae Carica papaya L. Papaya (Pawpaw) Tropaeolaceae Tropaeolum majus L. ‘Nasturtium’ (Indian cress) References are: Carlson et al. (1981), Fenwick et al. (1982), Carlson et al. (1987), Adams et al. (1989). OH R-C /s OH \\ N - OSO, Fig. 1. The general structure of glucosinolates. Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.22, on 24 Sep 2021 at 21:32:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1079/NRR19940012 GLUCOSINOLATES AND CANCER 207 Species belonging to these families are widely consumed by humans as cooked or salad vegetables (cabbage, Brussels sprouts, cauliflower, turnip, radish, cress) or condiments (horseradish, mustard, caper) ; cruciferous forages (kale, rape, turnip) and oilseed meals (rape, turnip rape) are used as feedstuffs for animals (Fenwick et al. 1982). More than 100 different GSL, which all share a common structure (Fig. l), have been identified so far (Fenwick et al. 1982). GSL may be classified into several chemical families according to their side groups R (Fenwick et al. 1986; Quinsac, 1993), which include alkyl, alkenyl, hydroxyalkyl, hydroxyalkenyl, methylthioalkyl, methylsulphinylalkyl, methyl- sulphonylalkyl, arylalkyl and indolyl groups (Table 2). Furthermore, a new family of GSL, designated cinnamoylGSL, was recently identified (Linscheid et al. 1980; Bjerg & Snrrensen, 1987). It differs from the usual pattern by the presence of cinnamic acid derivatives in the C(2) and/or C(6) positions on the glucose moiety. Edible plants may contain up to fifteen different GSL. However, most of them synthesize between one and five of these compounds. Concern about the potential biological effects of GSL has in the last decade prompted various groups to examine the levels and profiles of these compounds in cruciferous vegetables. The reader interested in detailed information is referred to the extensive research performed at the Northern Regional Research Center of the US Department ofAgriculture (Daxenbichler et al. 1979; Carhon et al. 1981,1985,1987) and at the Norwich Laboratory of the Institute of Food Research in Britain (Heaney & Fenwick, 1980a, b; Fenwick et al. 1982; Sones et al. 1984a, b; Lewis & Fenwick, 1987, 1988). Findings published by these and other workers are schematically summarized in Table 3. On the whole, great variations in the content as well as in the pattern of GSL occur according to the plant species. The wide range of GSL concentrations sometimes observed within an experiment and between different studies performed on the same vegetable indicates that further variations may occur according to the cultivar and the cultivation conditions. Carlson et al. (1985) have pointed out the remarkable differences in the GSL content between radishes originating from either the European-American or the Asian market. Analysis of Brussels sprouts and cauliflower cultivars grown at different sites in the UK shows great variations in the total GSL content (Heaney & Fenwick, 1980a, b; Sones efal. 19846); however, the relative proportions of the individual GSL tend to remain fairly stable within a cultivar. Climate, soil type and agronomic practices, especially fertilizer applications and harvest date, are cited as causative factors for such variations (Josefsson, 1970; Heaney & Fenwick, 1980a, b; Fenwick et al. 1982; Lehrmann, 1989; Booth et al. 1990). Another factor of tremendous importance is the part of the plant examined. Major quantitative and qualitative differences in the GSL accumulated by different organs (seeds, leaves, roots) and different tissues of the same organ (root peelings, cortex and medulla) occur in the same plant (Heaney & Fenwick, 1980a, b; Sang et al. 1984; Carlson et al. 1987; Adams et al. 1989). Such findings highlight the point that GSL biosynthesis in the plant is probably ruled by complex control mechanisms and that one cannot extrapolate data available for one part of the plant to another tissue. GENESIS OF GLUCOSINOLATE DERIVATIVES Enzymic hydrolysis and autolysis in cruciferous vegetables The breakdown of GSL by myrosinase, a specific plant hydrolytic enzyme (thioglucoside glucohydrolase EC 3.2.3. l), has been extensively studied and reviewed (Duncan & Milne, 1989). In intact cruciferous tissues, the enzyme is stored separately from the GSL substrates in specific cells named idioblasts. Contact between the two will result from mechanical injury Downloaded from https://www.cambridge.org/core. IP address: 170.106.33.22, on 24 Sep 2021 at 21:32:21, subject to the Cambridge Core terms of use, available at https://www.cambridge.org/core/terms. https://doi.org/10.1079/NRR19940012 208 L. NUGON-BAUDON AND SYLVIE RABOT Table 2. Glucosinolates occurring in edible plants Side chain Glucosinolate Trivial name CH3- methyl- glucocapparin CH3-CHr ethyl- glucolt5pidiin CHs-CH(CH3)- iso-propyl- glucoputranjivin CH&H>CH(CH3)- 1-methylpropyl- glucocochlearin CH~=CH-CHZ- prop-2-en yl- sinigrin CHZ=CH-CHZ-CH~- but-3-en yl- gluconapin CH~=CH-CHFCHZ-CH~- pent-4-eny l- glucobrassicanapin CH~=CH-CH(OH)-CHP (R)-2-hydroxybutd-enyl- progoitrin (S)-2-hydroxybut-3-enyl- epiprogoitrin CHZ=CH-CH~-CH(OH)-CH~- (R)-2-hydroxypent-4-enyl- gluconapoleiferin CH~-S-CHZ-CHZ-CHZ- J-methylthiopropyl- glucoiberverin CH&-CH~-CH~-CHTCH~- Cmethylthiobutyl- glucoerucin CH~-S-CH=CH-CH~-CHZ* 4-methylthiobut-3-enyl- glucoraphasatin CH~-S-CH~-CHZ-CH~-CH~-CH~-5 -methylthiopentyl- glucoberteroin CHrSO-CHrCHrCHr (R)-3-methylsulphinylpmpyl- glucoiberin CH~-SO-CHZ-CHTCHTCHZ- (R)-4-methylsulphinyIbutyl- glucoraphanin CH&O-CH=CH-CHZ-CH~- (R)-4-methylsulphinyIbut-3-enyl- glucoraphenin CH~-SO-CHZ-CHTCH~-CHZ-CH~(K)-5-methylsulphinylpentyl- glucoalyssin CH~-SO~-CHZ-CHZ-CH~* 3-methylsulphonylpropyl- glucocheirolin CHJ-S~~-CHTCH~CHZ-CHZ-4-methylsulphonylbutyl- glucoerysolin @-benzyl- glucotropaeolin 2-phenylethyl- gluconasturtiin pu+-\ (R)-2-hydroxy-2-phenylethyl- glucobarbarin @ (S)-P-hydroxy-2-phenylethyl- glucosibarin \p- J-hydroxybenzyl- glucolepigramin Ho +-4-hydroxybenzyl- sinalbin indol-3-ylmethyl-